The chemical brain hypothesis for the origin of nervous systems

Abstract

In nervous systems, there are two main modes of transmission for the propagation of activity between cells. Synaptic transmission relies on close contact at chemical or electrical synapses while volume transmission is mediated by diffusible chemical signals and does not require direct contact. It is possible to wire complex neuronal networks by both chemical and synaptic transmission. Both types of networks are ubiquitous in nervous systems, leading to the question which of the two appeared first in evolution. This paper explores a scenario where chemically organized cellular networks appeared before synapses in evolution, a possibility supported by the presence of complex peptidergic signalling in all animals except sponges. Small peptides are ideally suited to link up cells into chemical networks. They have unlimited diversity, high diffusivity and high copy numbers derived from repetitive precursors. But chemical signalling is diffusion limited and becomes inefficient in larger bodies. To overcome this, peptidergic cells may have developed projections and formed synaptically connected networks tiling body surfaces and displaying synchronized activity with pulsatile peptide release. The advent of circulatory systems and neurohemal organs further reduced the constraint imposed on chemical signalling by diffusion. This could have contributed to the explosive radiation of peptidergic signalling systems in stem bilaterians. Neurosecretory centres in extant nervous systems are still predominantly chemically wired and coexist with the synaptic brain. This article is part of the theme issue ‘Basal cognition: multicellularity, neurons and the cognitive lens’.

Elementary nervous systems

“…This hypothesis builds on the primacy of secretory cells as advocated by Lentz and others (see above), and is put forward for the first time in an elaborate fashion by Gáspár Jékely in this issue of Transactions [15]. Here, nervous system evolution starts from a sheet of ciliated cells.…”

“…Others envisaged effector cells carrying out immune functions in response to environmental microbes [12]. Finally, a strong camp emphasized the secretory nature of early neurons that may have acted at a distance on effector cells via the release of neuropeptides [13][14][15].…”

Reframing cognition: getting down to biological basics

“…Today, as several articles in Part 2 of this collection show [31–33], this supposition is now well-established and the focus of increasingly interesting research. For some, this ongoing reassessment has been destabilizing.…”

Multiple Origins of Neurons From Secretory Cells

“…The diversity of low molecular weight and peptide transmitters in all animals triggered several attempts to incorporate transmitter signaling in neuronal evolution models. Several recent publications provided different historical outlines and perspectives of this endeavor (Moroz, 2009 , 2014 ; Moroz and Kohn, 2015 , 2016 ; Arendt, 2021 ; Jekely, 2021 ; Moroz et al, 2021 ), which are not yet integrated into a comprehensive and unbiased review of the subject.…”